Article Figures & Data
Figures
- FIG. 1.
Distribution of different rrn operon numbers among bacterial (gray bars) and archaeal (black bars) isolates. Data were obtained from complete genome sequences from the NCBI and TIGR genome databases, the rrndb database, and the literature.
- FIG. 2.
Numbers (bars) and percentages of the total (line) of genomes with all identical 16S rRNA sequences among operons. Data were retrieved from the NCBI and TIGR genome databases and the rrndb database.
- FIG. 3.
Secondary structure model of the helices that differ in length between operons in Thermoanaerobacter tengcongensis. Nucleotide positions 444 to 490 (A) and 1,447 to 1,456 (B) are given according to Escherichia coli reference numbering.
Tables
- TABLE 1.
Number of operons, heterogeneity and redundancy of 16S rRNA genes within bacterial and archaeal genomes with multiple operonsa
Domain or microorganism Phylogenetic affiliation No. of operons No. of identical operonsb No. of different ribotypesc Nucleotide divergence (% 16S)d No. of poly- morph- ismse Source or referencef Bacteria (76 genomes) Aquifex aeolicus VF5 Aquificales 2 2 1 0 0 rrndb Chlorobium tepidum TLS Chlorobiales 2 2 1 0 0 This paper Synechocystis sp. PCC 6803 Cyanobacteria 2 2 1 0 0 This paper Treponema pallidum ATCC 25870 Spirochaetales 2 2 1 0 0 rrndb Leptospira interrogans serovar Lai 56601 Spirochaetales 2 2 1 0 0 This paper Caulobacter crecentus CB15 Alpha proteobacteria 2 2 1 0 0 This paper Xanthomonas axonopodis pv. citri 306 Gamma proteobacteria 2 2 1 0 0 This paper Xylella fastidiosa 9a5c Gamma proteobacteria 2 2 1 0 0 rrndb Xanthomonas campestris ATCC 33913 Gamma proteobacteria 2 2 1 0 0 This paper Helicobacter pylori 26695 Epsilon proteobacteria 2 2 1 0 0 rrndb Helicobacter pylori J99 Epsilon proteobacteria 2 0 2 ND ND 27 Ureaplasma urealyticum serovar 3 Mycoplasmatales 2 0 2 0.07 1 rrndb Mycobacterium celatum Actinomycetales 2 0 2 ND 4/5 34 Mycobacterium strain “X" Actinomycetales 2 0 2 1.20 18 30 Desulfotomaculum kuznestovii Clostridales 2 0 2 8.3 ND 40 Chlamydia trachomatis Chlamydiae 2 2 1 0 0 27 Geobacter sulfurreducens Delta proteobacteria 2 0/2 1/2 0/0.2 0/3 This paper Deincoccus radiodurans ATCC 13939 Deinococcales 3 2 2 0.13 2 rrndb Rhodobacter sphaeroides Alpha proteobacteria 3 3 1 0 0 10 Brucella suis 1330, biovar 1 Alpha proteobacteria 3 3 1 0 0 This paper Brucella melitensis 16M Alpha proteobacteria 3 3 1 0 0 This paper Sinorhizobium meliloti Alpha proteobacteria 3 3 1 0 0 This paper Ralstonia solanacearum Beta proteobacteria 3 3 1 0 0 This paper Campylobacter jenuni ATCC 700819 Epsilon proteobacteria 3 3 1 0 0 rrndb Nostoc sp. PCC 7120 Cyanobacteria 4 3 2 0.07 1 This paper Agrobacterium tumefaciens C58 Alpha proteobacteria 4 4 1 0 0 This paper Neisseria meningitidis MC58 Alpha proteobacteria 4 4 1 0 0 rrndb Pseudomonas aeruginosa PAO1 Gamma proteobacteria 4 2 + 2 2 0.07 1 This paper Enterococcus faecalis V583 Firmicutes 4 3 + 1 2 0.07 1 This paper Streptococcus pneumoniae R6 Firmicutes 4 4 1 0 0 This paper Streptococcus pneumoniae TIGR4 Firmicutes 4 4 1 0 0 This paper Thermobispora bispora R51 Actinomycetales 4 0 4 6.4 98 41 Thermoanaerobacter tengcongensis Thermoanaerobacteriales 4 0 4 6.5/11.6 99/188 This paper Pseudomonas syringae pv tomato DC3000 Gamma proteobacteria 5 5 1 0 0 This paper Fusobacterium nucleatum subsp. nucleatum Fusobacteria 5 2 + 1 + 1 + 1 4 0.20 3 This paper Corynebacterium efficiens YS-314 Actinomycetales 5 4 + 1 2 0.21/0.42 3/6 This paper Staphylococcus epidermidis ATCC 12228 Firmicutes 5 0 5 0.84 13 This paper Staphylococcus aureus N315 Firmicutes 5 2 + 1 + 1 + 1 4 0.25 4 This paper Staphylococcus aureus Mu50 Firmicutes 5 0 5 0.38 6 This paper Lactobacillus plantarum WCFS1 Firmicutes 5 2 + 2 + 1 3 0.13 2 This paper Streptococcus mutans UA159 Firmicutes 5 3 + 2 2 0.19 3 This paper Streptococcus pyogenes SSI-1 Firmicutes 5 5 1 0 0 This paper Clostridium tetani E88 Clostridiales 5 2 + 1 + 1 + 1 4 0.39 6 This paper Desulfovibrio vulgaris Delta proteobacteria 5 2 + 1 + 1 + 1 4 0.26 4 This paper Bacteroides thetaiotaomicron VPI-5482 Bacteroidales 5 2 + 2 + 1 3 1.23/1.3 17/18 This paper Haemophilus influenzae Rd (ATCC 51907) Gamma proteobacteria 6 6 1 0 0 rrndb Yersina pestis CO92 Gamma proteobacteria 6 2 + 1 + 1 + 1 + 1 5 0.27 4 This paper Corynebacterium glutamicum ATCC 13032 Actinomycetales 6 2 + 1 + 1 + 1 + 1 5 0.33/0.39 6 This paper Thermomonospora chromogena Actinomycetales 6 0 6 6 ND 43 Staphylococcus aureus MW2 Firmicutes 6 3 + 1 + 1 + 1 4 0.32 5 This paper Listeria monocytogenes EGD-e Firmicutes 6 2 + 2 + 1 + 1 4 0.32 5 This paper Listeria innocua Clip 11262 Firmicutes 6 5 + 1 2 0.25 4 This paper Lactococcus lactis subsp. lactis Firmicutes 6 5 + 1 2 0.06 1 This paper Streptococcus pyogenes MGAS315 Firmicutes 6 6 1 0 0 This paper Streptococcus pyogenes M1 GAS (SF370) Firmicutes 6 3 + 2 + 1 3 0.075/0.15 1/2 This paper Streptococcus pyogenes MGAS8232 Firmicutes 6 6 1 0 0 This paper Pseudomonas putida KT2440 Gamma proteobacteria 7 2 + 2 + 2 + 1 4 0.19 3 This paper Shigella flexneri 2a 301 Gamma proteobacteria 7 4 + 2 + 1 3 0.51/0.58 8/9 This paper Escherichia coli K-12 Gamma proteobacteria 7 3 + 1 + 1 + 1 + 1 5 1.23/1.36 18/21 This paper Escherichia coli EDL933 (O157:H7) Gamma proteobacteria 7 2 + 1 + 1 + 1 + 1 + 1 6 0.45/0.97 7/15 This paper Escherichia coli Sakai (O157:H7) Gamma proteobacteria 7 3 + 2 + 1 + 1 4 0.45/0.58 7/9 This paper Escherichia coli ATCC 10798 Gamma proteobacteria 7 3 + 1 + 1 + 1 + 1 5 1.23 19 rrndb Salmonella entercia serovar Typhimurium LT2 Gamma proteobacteria 7 3 + 1 + 1 + 1 + 1 5 0.64/0.58 9/10 This paper Salmonella enterica subs P. enterica serovar Typhi Gamma proteobacteria 7 3 + 2 + 1 + 1 4 0.13/0.19 2/3 This paper Salmonella enterica subs P. enterica serovar Typhi Ty2 Gamma proteobacteria 7 3 + 3 + 1 3 0.13/0.19 2/3 This paper Yersina pestis KIM10+ Gamma proteobacteria 7 5 + 2 2 0.06 1 This paper Oceanobacillus iheyensis HTE831 Firmicutes 7 3 + 1 + 1 + 1 + 1 5 0.96/1.02 15/16 This paper Streptococcus agalactiae NEM316 Firmicutes 7 6 + 1 2 0.07 1 This paper Streptococcus agalactiae 2603 V/R Firmicutes 7 7 1 0 0 This paper Vibrio cholerae El Tor N16961 Gamma proteobacteria 8 0 8 0.91/1.04 12/14 This paper Shewanella oneidensis MR-1 Gamma proteobacteria 9 4 + 3 + 1 + 1 4 0.32 5 This paper Bacillus subtilis 168 Firmicutes 10 0 10 1.48/2.18 23/34 This paper Clostridium perfringens 13 Clostridiales 10 0 10 0.93/1.18 14/18 37; this paper Vibrio parahaemolyticus (RIMB22106633) Gamma proteobacteria 11 2 + 2 + 2 + 1 + 1 + 1 + 1 + 1 8 0.61 9 This paper Clostridium acetobutylicum Clostridiales 11 7 + 1 + 1 + 1 +1 5 0.26/0.92 4/14 This paper Bacillus cereus ATCC 14579 Firmicutes 13 7 + 1 + 1 + 1 + 1 + 1 + 1 7 0.46 7 This paper Archaea (5 genomes) Methanocaldococcus jannaschii Methanococcales (Euryarchaeota) 2 0 2 0.07/0.27 1/4 rrndb; this paper Methanothermobacter thermoauto- trophicus Methanobacteriales (Euryarchaeota) 2 0 2 0.14 2 rrndb Haloarcula marismortui Halobacteriales (Euryarchaeota) 2 0 2 5 74 28 Methanosarcina acetivorans C2A Methanosarcinales (Euryarchaeota) 3 2 + 1 2 0.07 1 This paper Methanosarcina mazei Goe1 Methanosarcinales (Euryarchaeota) 3 3 1 0 0 This paper ↵a Data were obtained from the NCBI (www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html) and TIGR (www.tigr.org/tdb/mdbcomplete.html) genome databases, the rrndb (http://rrndb.cme.msu.edu) (22), and multiple literature sources.
↵b Different numbers indicate identical 16S rRNA gene sequences in genomes with multiple operons.
↵c Ribotypes are defined as identical 16S rRNA sequences.
↵d Divergence is represented by pairwise distances calculated from alignments of all 16S rRNA sequences for each genome. Single values indicate that there are no insertions or deletions (I/D). When two values are given, left values represent no I/D and right values are with I/D.
e The numbers of polymorphisms represent the cumulative numbers of sequence positions in which the aligned sequences differed. Single values indicate that there are no insertions or deletions (I/D). When two values are given, left values represent no I/D and right values are with I/D.
↵f ND, not determined. Analyses were performed on alignments generated for this paper unless other sources are listed.
- TABLE 2.
Strains of the same bacterial species with different numbers of rrn operonsa
Microorganism name Phylogenetic affiliation No. of rrn operon copies Borrelia burgdorferi Spirochaetales 1 and 2 Chlamydia trachomatis Chlamydiae 1 and 2 Rhodococcus fascians Actinomycetales 4 and 5 Rhodopseudomonas palustris Alpha proteobacteria 1 and 2 Bradyrhizobium japonicum Alpha proteobacteria 1 and 2 Vibrio parahaemolyticus Gamma proteobacteria 9 and 11 Vibrio cholerae Gamma proteobacteria 7, 8, and 9 Pasteurella multocida Gamma proteobacteria 5 and 6 Yersinia pestis Gamma proteobacteria 6 and 7 Bacillus subtilis Firmicutes 9 and 10 Bacillus anthracis Firmicutes 10 and 11 Bacillus cereus Firmicutes 9, 12, and 13 Staphylococcus aureus Firmicutes 5 and 6 Enterococcus faecium Firmicutes 5 and 6 Streptococcus agalactiae Firmicutes 6 and 7 Streptococcus pyogenes Firmicutes 5 and 6 ↵a Data were obtained from the NCBI genome database (http://www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html), the rrndb (http://rrndb.cme.msu.edu) (22), and the literature (18, 20).
- TABLE 3.
Range and averages of percentages of nucleotide divergence in bacterial 16S rRNA sequences within genomes with multiple rrn operonsa
No. of rrn operons No. of sequences Range of divergence (%) (−I/D) Average (%) (−I/D) Range of divergence (%) (+I/D) Average (%) (+I/D) 2b 15 0-1.2 0.09 0-1.2 0.1 3 7 0-0.13 0.018 0-0.13 0.018 4b 7 0-0.07 0.03 0-0.07 0.03 5 12 0-1.23 0.34 0-1.36 0.363 6b 10 0-0.33 0.162 0-0.39 0.176 7 13 0-1.23 0.396 0-1.36 0.487 8 2 0.91 0.91 1.04 1.04 9 1 0.32 0.32 0.32 0.32 10 3 0.97-1.48 1.15 0.97-2.18 1.46 11 2 0.26-0.61 0.435 0.61-0.92 0.765 12 1 0.33 0.33 0.33 0.33 13 2 NA NA NA NA 15 1 NA NA NA NA ↵a Data were obtained from the NCBI (www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html) and TIGR (www.tigr.org/tdb/mdb/mdbcomplete.html) genome databases, the rrndb (http://rrndb.cme.msu.edu) (22), and multiple literature sources. NA, no rrn operon sequences were available.
↵b Four cases of extreme divergence (sequences from microorganisms in which the percentage of nucleotide divergence was much higher than the average) were excluded from the calculation. These were Desulfotomaculum kuznestovii, with two rrn operons and an 8.3% difference, Thermobispora bispora R51 and Thermoanaerobacter tengcongensis, both with four rrn operons and 6.4 and 11.6% differences, respectively, and Thermonospora chromogena, with six rrn operons and 6% divergence.
